Hostname: page-component-586b7cd67f-g8jcs Total loading time: 0 Render date: 2024-11-22T21:13:14.716Z Has data issue: false hasContentIssue false
  • English
  • Français

The size and complexity of dolphin brains—a paradox?

Published online by Cambridge University Press:  17 March 2008

Stefan Huggenberger
Stefan Huggenberger*
Affiliation:
Zoological Institute II, University of Cologne, Weyertal 119, 50931 Köln, Germany
*
Correspondence should be addressed to: Stefan Huggenberger, Zoological Institute II, University of Cologne, Weyertal 119, 50931 Köln, Germany email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Dolphin brain size with respect to body size ranks between that of apes and humans. The hypertrophic auditory structures, the large cerebrum with extended gyrification and the highly cognitive capabilities of toothed whales seem to be in paradoxical contrast to their thin neocortex with a plesiomorphic or paedomorphic cytoarchitecture. The total number of neurons in the delphinid neocortex is comparable to that of the chimpanzee (Primates), but, in relation to body weight, in the magnitude of the hedgehog (Insectivora) neocortex since cetaceans may be able to obtain larger body sizes than terrestrial mammals due to reduced gravitational effects in water. During evolution, dolphins may have increased the computational performance of their cytoarchitectonically ‘simple’ neocortex by a multiplication of relevant structures (resulting in a hypertrophic surface area) instead of increasing its complexity. Based on this hypothesis, I suggest that the evolution of the large dolphin brain was possible due to a combination of different prerequisites based on adaptations to the aquatic environment including the sonar system. The latter facilitated a successful feeding strategy to support an increased metabolic turnover of the brain and led to a hypertrophic auditory system. Moreover, the rudimentary pelvic girdle did not limit brain size at birth. These adaptations favoured the evolutionary size increase of the cerebral cortex in dolphins facilitating highly cognitive capabilities as well as precise and rapid sound processing using a ‘simple’ kind of neocortical cytoarchitecture.

Keywords

neocortexauditory systemtoothed whalescognitive capabilities
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 88 , Special Issue 6: Marine Mammals , September 2008 , pp. 1103 - 1108
Copyright
Copyright © Marine Biological Association of the United Kingdom 2008

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

REFERENCES

Acevedo-Gutiérrez, A. (2002) Group behavior. In W.F., Perrin et al. (eds) Encyclopedia of marine mammals San Diego: Academic Press, pp. 537–544.Google Scholar
Adam, P.J. (2002) Pelvic anatomy. In W.F., Perrin et al. (eds) Encyclopedia of marine mammals San Diego: Academic Press, pp. 894–897.Google Scholar
Breathnach, A.S. (1960) The cetacean central nervous system. Biological Reviews 35, 187–230.CrossRefGoogle Scholar
Browne, D. (2004) Do dolphins know their own minds? Biology and Philosophy 19, 633–653.CrossRefGoogle Scholar
Bullock, T.H. and Gurevich, V. (1979) Soviet literature on the nervous system and psychobiology of Cetacea. International Review of Neurobiology 21, 48–127.Google ScholarPubMed
Connor, R.C. (2007) Dolphin social intelligence: complex alliance relationships in bottlenose dolphins and a consideration of selective environments for extreme brain size evolution in mammals. Philosophical Transactions of the Royal Society B 362, 587–602.CrossRefGoogle Scholar
Connor, R.C. and Mann, J. (2006) Social cognition in the wild: Machiavellian dolphins? In Hurley, S. and Nudds, M. (eds) Rational animals? Oxford: Oxford University Press, pp. 329–370.CrossRefGoogle Scholar
Connor, R.C., Mann, J., Tyack, P.L. and Whitehead, H. (1998) Social evolution in toothed whales. Trends in Ecology and Evolution 13, 228–232.CrossRefGoogle ScholarPubMed
Cranford, T.W. and Amundin, M. (2004) Biosonar pulse production in odontocetes: the state of our knowledge. In Thomas, J.A. et al. (eds) Echolocation in bats and dolphins. Chicago: University of Chicago Press, pp. 26–59.Google Scholar
Cranford, T.W., Amundin, M. and Norris, K.S. (1996) Functional morphology and homology in the odontocete nasal complex: implication for sound generation. Journal of Morphology 228, 223–285.3.0.CO;2-3>CrossRefGoogle ScholarPubMed
Deacon, T.W. (1990) Rethinking mammalian brain evolution. American Zoologist 30, 629–705.CrossRefGoogle Scholar
Eriksen, N. and Pakkenberg, B. (2007) Total neocortical cell number in the mysticete brain. Anatomical Record 290, 83–95.CrossRefGoogle ScholarPubMed
Fordyce, R.E. and de Muizon, C. (2001) Evolutionary history of the cetaceans: a review. In Mazin, J.M. and de Buffrénil, V. (eds) Secondary adaptation of tetrapods to life in water Munich: Verlag Dr Friedrich Pfeil, pp. 169–234.Google Scholar
Fung, C., Schleicher, A., Kowalski, T. and Oelschläger, H.H.A. (2005) Mapping auditory cortex in the La Plata dolphin (Pontoporia blainvillei). Brain Research Bulletin 66, 353–356.CrossRefGoogle Scholar
Glezer, I.I. (2002) Neural morphology. In Hoelzel, A.R. (ed.) Marine mammal biology: an evolutionary approach, Oxford: Blackwell Science, pp. 98–115.Google Scholar
Glezer, I.I., Jacobs, M.S. and Morgane, P.J. (1988) The “initial” brain concept and its implications for brain evolution in Cetacea. Behavioral and Brain Sciences 11, 75–116.CrossRefGoogle Scholar
Glezer, I.I. and Morgane, P.J. (1990) Ultrastructures of synapses and Golgi analysis of neurons in the neocortex of the lateral gyrus (visual cortex) of the dolphin and the pilot whale. Brain Research Bulletin 24, 401–427.CrossRefGoogle ScholarPubMed
Harvey, P.H. and Krebs, J.R. (1990) Comparing brains. Science 249, 140–146.Google Scholar
Haug, H. (1987) Brain sizes, surfaces, and neuronal sizes of the cortex cerebri: a stereological investigation of man and his variability and a comparison with some mammals (primates, whales, marsupials, insectivores, and one elephant). American Journal of Anatomy 180, 126–142.CrossRefGoogle Scholar
Herman, L.M. (2006) Intelligence and rational behaviour in the bottlenosed dolphin. In Hurley, S. and Nudds, M. (eds) Rational animals? Oxford: Oxford University Press, pp. 439–468.CrossRefGoogle Scholar
Hof, P.R.Chanis, R. and Marino, L. (2005) Cortical complexity in cetacean brains. Anatomical Record 287A, 1142–1152.CrossRefGoogle Scholar
Hof, P.R. and Gucht E., van der (2007) Structure of the cerebral cortex of the humpback whale, Megaptera novaeangliae (Cetacea, Mysticeti, Balaenopteridae). Anatomical Record 290, 1–31.CrossRefGoogle ScholarPubMed
Krützen, M., Mann, J., Heithaus, M.R., Connor, R.C., Bejdar, L. and Sherwin, W.B. (2005) Cultural transmission of tool use in bottlenose dolphins. Proceedings of the National Academy of Science of the United Stated of America 102, 8939–3943.CrossRefGoogle ScholarPubMed
Kuczaj, S.A., Makecha, R., Trone, M., Paulos, R.D. and Ramos, J.A. (2007) Role of peers in cultural innovation and cultural transmission: evidence from the play of dolphin calves. International Journal of Comparative Psychology 19, 223–240.Google Scholar
Langworthy, O.R. (1932) A description of the central nervous system of the porpoise (Tursiops truncatus). Journal of Comparative Neurology 54, 437–499.CrossRefGoogle Scholar
Leatherwood, S. and Reeves, R.R. (1983) The Sierra Club handbook of whales and dolphins. San Francisco: Sierra Club Books.Google Scholar
Lefebvre, L., Marino, L., Sol, D., Lemieux-Lefebvre, S. and Arshad, S. (2006) Large brains and lengthened life history periods in odontocetes. Brain, Behavior and Evolution 68, 218–228.CrossRefGoogle ScholarPubMed
Lusseau, D. and Newman, M.E. (2004) Identifying the role that animals play in their social networks. Proceedings of the Biological Sciences 271 (Suppl. 6), 477–481.Google Scholar
Manger, P.R. (2006) An examination of cetacean brain structure with a novel hypothesis correlating thermogenesis to the evolution of a big brain. Biological Reviews 81, 293–338.CrossRefGoogle Scholar
Marino, L. (1998) A comparison of encephalization between odontocete cetaceans and anthropoid primates. Brain, Behavior and Evolution 51, 230–238.CrossRefGoogle ScholarPubMed
Marino, L. (2002) Convergence in complex cognitive abilities in cetaceans and primates. Brain, Behavior and Evolution 59, 21–32.CrossRefGoogle ScholarPubMed
Marino, L. (2007) Cetacean brains: how aquatic are they? Anatomical Record 290, 694–700.CrossRefGoogle Scholar
Marino, L., McShea, D. and Uhen, M.D. (2004) The origin and evolution of large brains in toothed whales. Anatomical Record 281A, 1247–1255.Google Scholar
Marino, L., Uhen, M.D., Pyenson, N.D. and Frohlich, B. (2003) Reconstructing cetacean brain evolution using computed tomography. Anatomical Record 272B, 107–117.CrossRefGoogle Scholar
Marino, L. et al. (2007) Cetaceans have complex brains for complex cognition. PLoS Biology 5, e139. doi:10.1371/journal.pbio.0050139.CrossRefGoogle ScholarPubMed
McFarland, W.L., Jacobs, M.S. and Morgane, P.J. (1979) Blood supply to the brain of the dolphin, Tursiops truncatus, with comparative observations on special aspects of the cerebrovascular supply of other vertebrates. Neuroscience and Biobehavioral Reviews (Suppl. 1), 93.Google Scholar
Mooney, T.A., Nachtigall, P.E. and Yuen, M.M.L. (2006) Temporal resolution of the Risso's dolphin, Grampus griseus, auditory system. Journal of Comparative Physiology 192A, 373–380.CrossRefGoogle Scholar
Morgane, P.J., Glezer, I. and Jacobs, M.S. (1990) Comparative and evolutionary anatomy of the visual cortex of the dolphin. In Jones, E.G. and Peters, A. (eds) Comparative structures and evolution of cerebral cortex, New York: Plenum Press, pp. 215–262.Google Scholar
Nikaido, M., Piskurek, O. and Okada, N. (2007) Toothed whale monophyly reassessed by SINE insertion analysis: the absence of lineage sorting effects suggests a small population of a common ancestral species. Molecular Phylogenetics and Evolution 43, 216–224.CrossRefGoogle ScholarPubMed
Niven, J.E. (2005) Brain evolution: getting better all the time? Current Biology 15, R624–R626.CrossRefGoogle ScholarPubMed
Oelschläger, H.A. (1990) Evolutionary morphology and acoustics in the dolphin skull. In Thomas, J. and Kastelein, R.A. (eds) Sensory abilities of cetaceans. New York: Plenum Press, pp. 137–162.CrossRefGoogle Scholar
Oelschläger, H.H.A. (in press). The dolphin brain—a challenge for synthetic neurobiology. Brain Research Bulletin.Google Scholar
Oelschläger, H.H.A., Haas-Rioth, M., Fung, C., Ridgway, S.H. and Knauth, M. (2008) Morphology and evolutionary biology of the dolphin (Delphinus sp.) brain—MR imaging and conventional histology. Brain Behavior and Evolution 71, 68–86.CrossRefGoogle ScholarPubMed
Oelschläger, H.H.A. and Kemp, B. (1998) Ontogenesis of the sperm whale brain. Journal of Comparative Neurology 399, 210–228.3.0.CO;2-3>CrossRefGoogle ScholarPubMed
Oelschläger, H.H.A. and Oelschläger, J.S. (2002) Brain. In W.F., Perrin et al. (eds) Encyclopedia of marine mammals, San Diego: Academic Press, pp. 133–158.Google Scholar
Rauschmann, M.A., Huggenberger, S., Kossatz, L.S. and Oelschläger, H.H.A. (2006) Head morphology in perinatal dolphins: a window into phylogeny and ontogeny. Journal of Morphology 267, 1295–1315.CrossRefGoogle ScholarPubMed
Reiss, D. and Marino, L. (2001) Mirror self recognition in the bottlenose dolphin: a case of cognitive convergence. Proceedings of the National Academy of Science of the United Stated of America 98, 5937–5942.Google Scholar
Rendell, L. and Whitehead, H. (2001) Culture in whales and dolphins. Behavioral and Brain Sciences 24, 309–382.Google Scholar
Rice, D.W. (1998) Marine mammals of the world: systematics and distribution (Special Publication no. 4, Society for Marine Mammalogy). Lawrence: Allen Press.Google Scholar
Ridgway, S.H. (1986) Physiological observations on dolphin brains. In Schusterman, R.J. et al. (eds) Dolphin cognition and behavior: a comparative approach, Hillsdale NJ: Lawrence Erlbaum Associates, pp. 31–59.Google Scholar
Ridgway, S.H. (1990) The central nervous system of the bottlenose dolphin. In Leatherwood, S. and Reeves, R. (eds) The bottlenose dolphin, New York: Academic Press, pp. 69–97.CrossRefGoogle Scholar
Ridgway, S.H. (2000) The auditory central nervous system of dolphins. In W.W.L., Au et al. (eds) Hearing by whales and dolphins, New York: Springer, pp. 273–294.Google Scholar
Ridgway, S.H. and Au, W.W.L. (1999) Hearing and echolocation: dolphin. In Adelman, G. and Smith, B.H. (eds) Elsevier's encyclopedia of neuroscinece 2nd edn, New York: Elsevier Science, pp. 858–862.Google Scholar
Ridgway, S.H. and Brownson, R.H. (1979) Brain size and symmetry in three dolphin genera. Anatomical Record 193, 664.Google Scholar
Ridgway, S.H. and Brownson, R.H. (1984) Relative brain sizes and cortical surface areas of odontocetes. Acta Zoologica Fennica 172, 149–152.Google Scholar
Ridgway, S.H. et al. (2006) Functional imaging of dolphin brain metabolism and blood flow. Journal of Experimental Biology 209, 2902–2910.CrossRefGoogle ScholarPubMed
Roth, G. and Dicke, U. (2005) Evolution of the brain and intelligence. Trends in Cognitive Sciences 9, 250–257.CrossRefGoogle ScholarPubMed
Ruff, C.B. (1995) Biomechanics of the hip and birth in early Homo. American Journal of Physical Anthropology 98, 527–574.CrossRefGoogle ScholarPubMed
Schwerdtfeger, W.K., Oelschläger, H.A. and Stephan, H. (1984) Quantitative neuroanatomy of the brain of the La Plata dolphin, Pontoporia blainvillei. Anatomy and Embryology 170, 11–19.CrossRefGoogle Scholar
Shoshani, J., Kupsky, W.J. and Marchant, G.H. (2006) Elephant brain—Part I: gross morphology, functions, comparative anatomy, and evolution. Brain Research Bulletin 70, 124–157.CrossRefGoogle ScholarPubMed
Simmonds, M.P. (2006) Into the brains of whales. Applied Animal Behaviour Science 100, 103–116.Google Scholar
Spector, W.S. (1956) Handbook of biological data. Philadelphia and London: Saunders.Google Scholar
Tyack, P.L. (2002) Behavior, overview. In W.F., Perrin et al. (eds) Encyclopedia of marine mammals San Diego: Academic Press, pp. 87–94.Google Scholar
Wood, E.G. and Evans, W.E. (1980) Adaptiveness and ecology of echolocation in toothed whales. In Busnel, R. and Fish, J. (eds) Animal sonar systems, New York: Plenum Press, pp. 381–426.CrossRefGoogle Scholar
Würsig, B. (2002) Intelligence and cognition. In W.F., Perrin et al. (eds) Encyclopedia of marine mammals San Diego: Academic Press, pp. 628–637.Google Scholar