The widespread variation in brain size and complexity that is evident in sharks and holocephalans is related to both phylogeny and ecology. Relative brain size (expressed as encephalization quotients) and the relative development of the five major brain areas (the telencephalon, diencephalon, mesencephalon, cerebellum, and medulla) was assessed for over 40 species from 20 families that represent a range of different lifestyles and occupy a number of habitats. In addition, an index (1–5) quantifying structural complexity of the cerebellum was created based on length, number, and depth of folds. Although the variation in brain size, morphology, and complexity is due in part to phylogeny, as basal groups have smaller brains, less structural hypertrophy, and lower foliation indices, there is also substantial variation within and across clades that does not reflect phylogenetic relationships. Ecological correlations, with the relative development of different brain areas as well as the complexity of the cerebellar corpus, are supported by cluster analysis and are suggestive of a range of ‘cerebrotypes’. These correlations suggest that relative brain development reflects the dimensionality of the environment and/or agile prey capture in addition to phylogeny.

Keywords:
Allometry, Ecomorphology, Nervous system, Cerebellum, Morphometrics, Neuromorphology, Comparative brain morphology, Chondrichthyan
1.
Albus JS (1971) A theory of cerebellar function. Math Biosci 10:25–61.
2.
Armstrong RH (1996) Alaska’s Fish. A guide to selected species. Alaska: Alaska Northwest Books.
3.
Bard P, Macht MB (1958) The behavior of chronically decerebrate cat. In: Neurological Basis of Behavior (Wolstenholme GEW, O’Connor CM, eds), pp 55–71. London: Churchill.
4.
Barton RA, Harvey PH (2000) Mosaic evolution of brain structure in mammals. Nature 405:1055–1058.
5.
Barton RA, Purvis A, Harvey PH (1995) Evolutionary radiation of visual and olfactory brain systems in primates, bats and insectivores. Phil Trans R Soc Lond B 348:381–392.
6.
Bastian AJ, Martin TA, Keating JG, Thach WT (1996) Cerebellar ataxia: abnormal control of interaction torques across multiple joints. J Neurophysiol 76:492–509.
7.
Bauchot R, Bauchot ML, Platel R, Ridet JM (1977) The brains of Hawaiian tropical fishes: Brain size and evolution. Copeia 1:42–46.
8.
Bauchot R, Platel R, Ridet JM (1976) Brain-body weight relationships in Selachii. Copeia 2:305–310.
9.
Bauchot R, Ridet JM, Bauchot ML (1989) The brain organization of butterflyb fishes. In: Environmental Biology of Fishes (Balon EK, Motta PJ, eds), pp 205–219. Dordrecht: Kluwer Academic Publishers.
10.
Brabrand A (1985) Food of roach (Rutilus rutilus) and ide (Leuciscus idus): Significance of diet shifts for interspecific competition in omnivorous fishes. Oecologia 66:461–467.
11.
Brandstätter R, Kotrschal K (1990) Brain growth patterns in four European cyprinid fish species (Cyprinidae, Teleostei): roach (Rutilus rutilus), bream (Abramis brama), common carp (Cyprinus carpio) and sabre carp (Pelecus cultratus). Brain Behav Evol 35:195–211.
12.
Budeau DA, Verts BJ (1986) Relative brain size and structural complexity of habitats of chipmunks. J Mammal 67:579–581.
13.
Butler AB (2003) Sensory systems and brain evolution across the Bilateria: Commonalities and constraints. In: Sensory Processing in Aquatic Environments. (Collin SP, Marshall NJ, eds), pp 375–388. New York: Springer-Verlag.
14.
Carrier JC, Musick JA, Heithaus MR (eds) (2004) Biology of Sharks and Their Relatives. New York: CRC Press.
15.
Clark DA, Mitra PP, Wang SS-H (2001) Scalable architecture in mammalian brains. Nature 411:189–193.
16.
Compagno LJV (1973) Interrelationships of living elasmobranchs. In: Interrelationships of Fishes (Greenwood RSM, Patterson C, eds), pp 15–61. London: Academic Press.
17.
Compagno LJV (1977) Phyletic relationships of living sharks and rays. Am Zool 17:303–322.
18.
Compagno LJV (1984a) FAO Species Catalogue. Sharks of the World. An annotated and illustrated catalogue of shark species known to date. I. Hexanchiformes to Lamniformes. Vol 4. Rome: FAO Fisheries Synopsis.
19.
Compagno LJV (1984b) FAO Species Catalogue. Sharks of the world. An annotated and illustrated catalogue of shark species known to date. II. Carcharhiniformes. Vol 4. Rome: FAO Fisheries Synopsis.
20.
Compagno LJV (1988) Sharks of the Order Carcharhiniformes. Princeton NJ: Princeton University Press.
21.
Compagno LJV (1998) Lamnidae. Mackerel sharks, makos, white sharks, porbeagles. In: FAO Identification Guide for Fishery Purposes. The Living Marine Resources of the Western Central Pacific (Carpenter KE, Niem VH, eds), pp 1274–1278. Rome: FAO Fisheries Synopsis.
22.
Compagno LJV (1999) Checklist of living elasmobranches. In: Sharks, Skates, & Rays. The Biology of Elasmobranch Fishes (Hamlet WC, ed), pp 471–498. Baltimore, MD: The Johns Hopkins University Press.
23.
Compagno LJV (2001) Sharks of the World. An annotated and illustrated catalogue of shark species known to date. Bullhead, mackerel and carpet sharks (Heterodontiformes, Lamniformes and Orectolobiformes). Vol 2. Rome: FAO Fisheries Synopsis.
24.
Compagno LJV, Ebert DA, Smale MJ (1989) Guide to the sharks and rays of southern Africa. London: New Holland Ltd.
25.
Compagno LJV, Niem VH (1998a) Carcharhinidae. Requiem sharks. In: FAO Identification Guide for Fishery Purposes. The Living Marine Resources of the Western Central Pacific (Carpenter KE, Niem VH, eds), pp 1312–1360. Rome: FAO Fisheries Synopsis.
26.
Compagno LJV, Niem VH (1998b) Squalidae. Dogfish sharks. In: FAO Identification Guide for Fishery Purposes. The Living Marine Resources of the Western Central Pacific (Carpenter KE, Niem VH, eds), pp 1213–1232. Rome: FAO Fisheries Synopsis.
27.
Cortés E (1999) Standardized diet compositions and trophic levels of sharks. ICES J Marine Sci 56:707–717.
28.
de Carvalho MR (1996) Higher-level elasmobranch phylogeny, basal squaleans, and paraphyly. In: Interrelationships of Fishes (Stiassny MLJ, Parenti LR, Johnson GD, eds), pp 35–62. San Diego, CA: Academic Press.
29.
de Winter W, Oxnard CE (2001) Evolutionary radiations and convergences in the structural organization of mammalian brains. Nature 409:710–714.
30.
Demski LS, Northcutt RG (1996) The brain and cranial nerves of the white shark: an evolutionary perspective. In: Great White Sharks: the Biology of Carcharodon carcharias (Klimley AP, Ainley DG, eds), pp 121–130. San Diego, CA: Academic Press.
31.
Didier DA (2004) Phylogeny and classification of extant Holocephali. In: Biology of Sharks and Their Relatives (Carrier JC, Musick JA, Heithaus MR, eds), pp 115–135. New York: CRC Press.
32.
Donley JM, Shadwick RE (2003) Steady swimming muscle dynamics in the leopard shark Triakis semifasciata. J Exp Biol 206:1117–1126.
33.
Dunn KA, Morrissey JF (1995) Molecular phylogeny of elasmobranchs. Copeia 3:526–531.
34.
Earhart GM, Bastian AJ (2000) Form switching during human locomotion: traversing wedges in a single step. J Neurophysiol 84:605–615.
35.
Earhart GM, Bastian AJ (2001) Selection and coordination of human locomotor forms following cerebellar damage. J Neurophysiol 85:759–769.
36.
Eisenberg JF, Wilson DE (1978) Relative brain size and feeding strategies in the Chiroptera. Evolution 32:740–751.
37.
Felsenstein J (1985) Phylogenies and the comparative method. Am Nat 125:1–15.
38.
Gao JH, Parsons LM, Bower JM, Xiong J, Li J, Fox PT (1996) Cerebellum implicated in sensory acquisition and discrimination rather than motor control. Science 272:545–547.
39.
Garland T, Harvey PH, Ives AR (1992) Procedures for the analysis of comparative data using phylogenetically independent contrasts. Syst Biol 41:18–32.
40.
Garman S (1913) The Plagiostomia (Sharks, Skates, and Rays). Vol XXXVI. Cambridge, MA: Harvard College.
41.
Gelfand MJ, O’Hara SM, Curtwright LA, MacLean JR (2005) Pre-medication to block [F-18] FDG uptake in the brown adipose tissue of pediatric and adolescent patients. Pediatr Radiol 35:984–990.
42.
Gluck MA, Allen MT, Myers CE, Thompson RF (2001) Cerebellar substrates for error correction in motor conditioning. Neurobiol Learn Mem 76:314–341.
43.
Gordon AM, Westling G, Cole KJ, Johansson RS (1993) Memory representations underlying motor commands used during manipulation of common and novel objects. J Neurophysiol 69:1789–1796.
44.
Goto T (2001) Comparative anatomy, phylogeny and cladistic classification of the order Orectolobiformes (Chondrichtyes, Elasmobranchii). Mem Grad Sch Fish Sci Hokkaido Univ 48:1–100.
45.
Gruber SH, Myrberg AAJ (1977) Approaches to the study of the behavior of sharks. Am Zool 17:471–486.
46.
Harvey MJ, Krebs JR (1990) Comparing brains. Science 249:140–146.
47.
Harvey PH, Pagel MD (1991) The Comparative Method in Evolutionary Biology. Oxford, UK: Oxford University Press.
48.
Hildebrand M (2001) Nervous System: Brain. In: Analysis of Vertebrate Structure (Hildebrand M, Goslow G, eds), pp 319–344. New York: John Wiley and Sons, Inc.
49.
Hofmann MH (1999) Nervous System. In: Sharks, Skates, & Rays: The Biology of Elasmobranch Fishes (Hamlet WC, ed), pp 273–299. Baltimore, MD: Johns Hopkins University Press.
50.
Huber R, Rylander MK (1992) Brain morphology and turbitity preference in Notropis and related genera (Cyprinidae, Teleostei). In: Environmental Biology of Fishes (Balon EK, Weiser W, Schiemer F, Goldschmidt A, Kotrschal K, eds), Vol 33, pp 153–165. Dordrecht: Kluwer Academic Publishers.
51.
Huber R, van Staaden MJ, Kaufman LS, Liem KF (1997) Microhabitat use, trophic patterns and the evolution of brain structure in African cichlids. Brain Behav Evol 50:167–182.
52.
Hutcheon JM, Kirsch JW, Garland T (2002) A comparative analysis of brain size in relation to foraging ecology and phylogeny in the Chiroptera. Brain Behav Evol 60:165–180.
53.
Ito H, Yoshimoto M, Somiya H (1999) External brain form and cranial nerves of the megamouth shark, Megachasma pelagios. Copeia 1999:210–213.
54.
Ito M (1984) The Cerebellum and Neural Control. New York: Raven Press.
55.
Iwaniuk AN, Hurd PL (2005) The evolution of cerebrotypes in birds. Brain Behav Evol 65:215–230.
56.
Jerison HJ (1973) Evolution of the Brain and Intelligence. New York: Academic Press.
57.
Johnson RH, Nelson DR (1973) Agonistic display in the gray reef shark, Carcharhinus menisorrah, and its relationship to attacks on man. Copeia 1973:76–84.
58.
Kappers CUA, Huber GC, Crosby E (1936) The Comparative Anatomy of the Nervous System of Vertebrates, Including Man. New York: Macmillan.
59.
Kim SJ, Kim IJ, Bae YT, Kim YK, Kim DS (2004) Objective interpretation of severity of SLS induced edema by stereoimaging. Eur J Radiol 53:192–198.
60.
Klimley AP (1985) Schooling in Sphyrna lewini, a species with a low risk of predation: a non-egalitarian state. J Comp Ethol 70:297–319.
61.
Kotrschal K, Palzenberger M (1992) Neuroecology of cyprinids: comparative, quantitative histology reveals diverse brain patterns. Environ Biol Fish 33:135–152.
62.
Kotrschal K, van Staaden MJ, Huber R (1998) Fish brains: evolution and environmental relationships. Rev Fish Biol Fish. 8:373–408.
63.
Kruska DCT (1988) The brain of the basking shark (Cetorhinus maximus). Brain Behav Evol 32:353–363.
64.
Kudo H, Dunbar RIM (2001) Neocortex size and social network size in primates. Anim Behav 62:711–722.
65.
Lackner JR, Dizio P (1994) Rapid adaptation to coriolis force perturbations of arm trajectory. J Neurophysiol 72:299–313.
66.
Lammens EHRR, Geursen J, McGillavry PJ (1987) Diet shifts, feeding efficiency and coexistence of bream (Abramis brama), roach (Rutilus rutilus) and white bream (Blicca bjoercna) in hypertrophic lakes. In: Proceedings of the V Congress of European Ichthyologists (Kullander S, Fernholm B, eds), pp 153–162. Stockholm: V Congress of European Ichthyologists.
67.
Lang CE, Bastian AJ (1999) Cerebellar subjects show impaired adaptation of anticipatory EMG during catching. J Neurophysiol 82:2108–2119.
68.
Larsell O (1967) The comparative anatomy and histology of the cerebellum from myxinoids through birds. Minneapolis, MN: The University of Minnesota Press.
69.
Last PR, Stevens JD (1994) Sharks and Rays of Australia. Melbourne: CSIRO.
70.
Lefebvre L, Gaxiola A, Dawson S, Timmermans S, Rosza L, Kabai P (1998) Feeding innovations and forebrain size in Australasian birds. Behaviour 135:1077–1097.
71.
Lefebvre L, Nicolakakis N, Boire D (2002) Tools and brains in birds. Behaviour 139:939–973.
72.
Lisney TJ, Collin SP (2006) Brain morphology in large pelagic fishes: a comparison between sharks and teleosts. J Fish Biol 68: 532–554.
73.
Long DJ (1991) Apparent predation by a white shark Carcharodon carcharias on a pygmy sperm whale Kogia breviceps. Fish Bull 89:538–540.
74.
Maisey JG (1984) Higher elasmobranch phylogeny and biostratigraphy. J Linn Soc 82:33–54.
75.
Maisey JG, Naylor GJP, Ward DJ (2004) Mesozoic elasmobranchs, neoselachian phylogeny and the rise of modern elasmobranch diversity. In: Mesozoic Fishes 3 – Systematics, Paleoenvironments and Biodiversity (Arratia G, Tintori A, eds), pp 17–56. München: F. Pfeil.
76.
Marr D (1969) A theory of cerebellar cortex. J Physiol 202:437–470.
77.
Martin AP, Naylor GJP, Palumbi SR (1992) Rates of mitochondrial DNA evolution in sharks are slow compared with mammals. Nature 357:153–155.
78.
Martin RD (1996) Scaling of the mammalian brain: the maternal energy hypothesis. News Physiol Sci 11:149–156.
79.
Masai H (1969) The brain patterns of sharks in relation to habit. J Hirnforsch 11:347–365.
80.
McEachran JD, Dunn KA, Miyake T (1996) Interrelationships of the batoid fishes (Chondrichthyes: Batoidea). In: Interrelationships of Fishes (Stiassny MLJ, Parenti LR, Johnson GD, eds), pp 63–84. San Diego CA: Academic Press.
81.
Montgomery J, Carton G, Bodznick D (2002) Error-driven motor learning in fish. Biol Bull 203:238–239.
82.
Myagkov NA (1991) The brain sizes of living Elasmobranchii as their organization level indicator. I. General Analysis. J Hirnforsch 32:553–561.
83.
Myrberg AAJ, Gruber S (1974) The behavior of the bonnethead shark, Sphyrna tiburo. Copeia 1974:358–374.
84.
Narendra KS (1990) Adaptive control using neural networks. In: Neural Networks for Control (Miller WT, Sutton RS, Werbos PJ, eds), pp 115–142. Cambridge, MA: MIT Press.
85.
Naylor GJP (1992) The phylogenetic relationships among requiem and hammerhead sharks: inferring phylogeny when thousands of equally most parsimonious trees result. Cladistics 8:295–318.
86.
New JG (2001) Comparative neurobiology of the elasmobranch cerebellum: theme and variations on a sensorimotor interface. Environ Biol Fish 60:93–108.
87.
Northcutt RG (1977) Elasmobranch central nervous system organization and its possible evolutionary significance. Am Zool 17:411–429.
88.
Northcutt RG (1978) Brain organization in the cartilaginous fishes. In: Sensory Biology of Sharks, Skates, and Rays (Hodgson ES, Mathewson RF, eds), pp 117–194. Arlington, VA: Office of Naval Research.
89.
Northcutt RG (1989) Brain variation and phylogenetic trends in elasmobranch fishes. J Exp Zool Suppl 2:83–100.
90.
Okada Y, Aoki M, Sato Y, Masai H (1969) The brain patterns of sharks in relation to habit. J Hirnforsch 11:347–365.
91.
Paul DH, Roberts BL (1979) The significance of cerebellar function for a reflex movement of the dogfish. J Comp Physiol 134:69–74.
92.
Paulin MG (1993) The role of the cerebellum in motor control and perception. Brain Behav Evol 41:39–51.
93.
Pirlot P, Jolicoeur P (1982) Correlations between major brain regions in Chiroptera. Brain Behav Evol 20:172–181.
94.
Purvis A, Rambaut A (1995a) Comparative Analysis by Independent Contrasts (CAIC): a statistical package for the Apple Macintosh. User’s Guide.
95.
Purvis A, Rambaut A (1995b) Comparative Analysis by Independent Contrasts (CAIC): an Apple Macintosh application for analyzing comparative data. Comp Appl Biosci 11:247–251.
96.
Riddell WI, Corl KG (1977) Comparative investigation and relationship between cerebral indices and learning abilities. Brain Behav Evol 14:305–308.
97.
Ritter EK, Godknecht AJ (2000) Agonistic displays in the blacktip shark (Carcharhinus limbatus). Copeia 2000:282–284.
98.
Schellart NAM, Prins M (1993) Interspecific allometry of the teleost visual system: a new approach. Neth J Zool 43:274–295.
99.
Schiemer F (1988) Gefährdete Cypriniden – Indikatoren für die ökologische Intaktheit von Fluβsystemen. Natur und Landschaft 63:370–373.
100.
Shadmehr R, Musso-Ivaldi FA (1994) Adaptive representation of dynamics during learning of a motor task. J Neurosci 14:3208–3224.
101.
Shirai S (1992a) Phylogenetic relationships of the angel sharks, with comments on elasmobranch phylogeny (Chondrichthyes, Squatinidae). Copeia 1992:505–518.
102.
Shirai S (1992b) Squalean phylogeny: a new framework of ‘squaloid’ sharks and related taxa. Sapporo: Hokkaido University Press.
103.
Shirai S (1996) Phylogenetic interrelationships of neoselachians (Chondrichthyes: Euselachii). In: Interrelationships of Fishes (Stiassny MLJ, Parenti LR, Johnson GD, eds), pp 9–34. San Diego, CA: Academic Press.
104.
Smale MJ (1996) Cephalopods as prey. IV. Fishes. Phil Trans R Soc Lond B 351:1067–1081.
105.
Smeets WJAJ (1998) Cartilaginous fishes. In: The Central Nervous System of Vertebrates (Nieuwenhuys R, Roberts BL, eds), pp 551–654. Berlin: Springer-Verlag.
106.
Smeets WJAJ, Nieuwenhuys R, Roberts BL (1983) The Central Nervous System of Cartilaginous Fishes: Structural and Functional Correlations. New York: Springer-Verlag.
107.
Springer S (1967) Social organization of shark populations. In: Sharks, Skates and Rays (Gilbert PW, Mathewson RF, Rall DP, eds), pp 149–174. Baltimore, MD: Johns Hopkins Press.
108.
Striedter GF (2005) Principles of Brain Evolution. Sunderland, MA: Sinauer Associates, Inc.
109.
Sultan F (2002) Analysis of mammalian brain architecture. Nature 415:133–134.
110.
Wagner HJ (2001a) Brain areas in abyssal demersal fishes. Brain Behav Evol 57:301–316.
111.
Wagner HJ (2001b) Sensory brain areas in mesopelagic fishes. Brain Behav Evol 57:117–133.
112.
Wagner HJ (2002) Sensory brain areas in three families of deep-sea fish (slickheads, eels and grenadiers): comparison of mesopelagic and demersal species. Marine Biol 141:807–817.
113.
Webb PW, Keyes RS (1982) Swimming kinematics of sharks. Fish Bull 80:803–812.
114.
Wilga CAD, Lauder GV (2004) Biomechanics of locomotion in sharks, rays, and chimaeras. In: Biology of Sharks and Their Relatives (Carrier JC, Musick JA, Heithaus MR, eds), pp 139–202. London: CRC Press.
115.
Williams JR, Babcock RC (2004) Comparison of multiple techniques to evaluate reproductive variability in a marine bivalve: application to the scallop Pecten novaezelandiae. Marine Fresh Res 55:457–468.
116.
Winchell CJ, Martin AP, Mallatt J (2004) Phylogeny of elasmobranchs based on LSU and SSU ribosomal RNA genes. Mol Phylogenet Evol 31:214–224.
117.
Wourms JP (1977) Reproduction and development in chondrichthyan fishes. Am Zool 17:379–410.
© 2007 S. Karger AG, Basel
2007
Copyright / Drug Dosage / Disclaimer
Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in government regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.
You do not currently have access to this content.