Mammalogy

Food for thought

Mormyrids (elephant-nose fishes)

Brain evolution

gnathonemus.jpg

Lateral view (left side) of Gnathonemus petersii (Mormyridae)
(© RMCA)

The African mormyrids or elephant-nose fishes were noted for having unusually large brains already more than a century ago (Erdl, 1846). 

For a mean body mass of 26 g, the mean brain weight of Gnathonemus petersii reaches 0.53 g, almost three times its expected mean value of 0.19 g, as calculated from the relationship between brain size and body size in teleost fish (Kaufman, 2003). 

This character is probably, at least in part, related to their ability to sense prey and to communicate by generating and perceiving electric fields (Nieuwenhuys and Nicholson, 1969).  In contrast with mammals, it is the cerebellum, and not the telencephalon that is greatly enlarged in these fishes.  More precisely, the most enlarged part of the mormyrids cerebellum (or “gigantocerebellum”, Nieuwenhuys and Nicholson, 1969) is the valvulla cerebelli (fig. 2).  This rostral protrusion of the cerebellum is only present in actinopterygian fish.  In elephant-nose fishes, the valvula cerebelli covers most of the rest of the brain (fig. 2).  In contrast, in another highly derived brain such as the human brain, it is the telencephalon, and more specifically the neocortex, a telencephalic structure unique to mammals, that entirely covers the rest of the brain (fig. 3).

image brain Gnathonemus petersii image brain Homo

Fig. 2. Parasagittal cresyl violet stained section through the brain of a Gnathonemus petersii showing the topography of the valvulla cerebelli covering most of the rest of the brain. 
“Brain” on this figure includes, from left to right, parts of the telencephalon, diencephalon and mesencephalon
(image realized by E. Gilissen on the material of Prof. J.M. Allman, Caltech, USA).

Fig. 3. Midsagittal magnetic resonance scan through a human head showing the topography of the most enlarged part of the human telencephalon, the neocortex, covering the rest of the brain, including the cerebellum.
(courtesy Prof. E.A. Cabanis, CHNO XV-XX, Paris).

 

image brain evolution
Fig. 4. Dorsal views of brains of selected vertebrates. 
Above right, last picture: The green structure is a chimpanzee brain (the only visible structure is the neocortex, which covers the brain entirely). 
Above left: the orange structure is the cerebellum, covering the brain entirely in elephant-nose fish (valvulla cerebelli) 
(ã Springer-Verlag Berlin Heidelberg (1998) R. Nieuwenhuys, H.J. ten Donkelaar, C. Nicholson. The Central Nervous System of Vertebrates).

 

Mormyrids therefore show an alternative way of evolving brains, radically different from the brain evolution driven by neocortex expansion, as illustrated in primate and especially human evolution (fig. 4).

The cost of brains

Brains are always costly organs in terms of energy consumption.  What are then the challenges faced by humans and mormyrids? 

Vertebrates show remarkably constant ratios of brain to body O2 consumption, the brain using 2–8 % of resting body O2 consumption, suggesting that evolution has put limits on the energetic cost of brain functions (Mink et al., 1981).  Only man is an exception to this rule.  The adult human brain accounts for 2% of the total body mass but consumes some 20 % of the O2 taken up by the resting body.  This represents an exceptionally high rate of energy use among vertebrates and appears to have remained undisputed. 
The results of Nilsson (1996) however suggest that, in the electric fish Gnathonemus petersii, the brain is responsible for approximately 60% of body O2 consumption, a figure three times higher than that for any other vertebrate studied so far, including human.

The exceptionally high energetic cost of the Gnathonemus petersii brain appears to be a consequence both of the brain being very large and of the fish being ectothermic (Nilsson, 1996).  At the same temperature and body size, total energy expenditures of ectothermic vertebrates are about 1/13 of those of endotherms but brain energy expenditures are quite similar.  When considering the whole-body energy budget, it is thus comparatively more expensive for an ectothermic vertebrate to have a large brain. This may be a reason why most ectothermic vertebrates have relatively small brains. 

Consequently, the fact that Gnathonemus petersii is an ectothermic vertebrate and has such a huge brain makes this organ an exceptionally expensive part of the whole body (Nilsson, 1996).  To some extent, Gnathonemus petersii therefore faces an ecophysiological challenge unparalled in the animal kingdom, including human.

Many thanks to Tobias Musschoot (Ichthyology RMCA) for his comments on a previous version of this text.

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References

Bullock, T.H. and Heiligenberg, W. (1986) Electroreception. In Wiley Series in Neurobiology (ed. R. G. Northcutt). New York: John Wiley & Sons Inc. 722pp

Erdl, M.P. (1846) Über das Gehirn der Fischgattung Mormyrus. Gelehrte Anzeigen der königlichen bayerischen Akademie der Wissenschaften. 22/23: 403-407

Hopkins, C.D. (1999) Design features for electric communication. The Journal of Experimental Biology 202: 1217–1228

Kaufman, J.A. (2003) On the expensive-tissue hypothesis: independent support from highly encephalized fish and reply by Hladik, C.M. and Pasquet, P. Current Anthropology 44: 705-707

Mink, J.W; Blumenschine, R.J.; Adams, D.B. (1981) Ratio of central nervous system activity to body metabolism in vertebrates: its constancy and functional basis. American Journal of Physiology 241: R203-R212

Moller, P. (1995) Electric fishes: history and behavior. In Chapman & Hall Fish and Fisheries Series, vol. 17 (ed. T. J. Pitcher). London, New York: Chapman & Hall. 584pp

Nelson, J.S. (2006) Fishes of the World. Fourth Edition. New Jersey: John Wiley & Sons. 601pp

Nieuwenhuys, R. and Nicholson, C. (1969) A survey of the general morphology, the fiber connections and the possible functional significance of the gigantocerebellum of mormyrid fishes. In: Neurobiology of Cerebellar Evolution and Development (ed. R. Llinás). Chicago: American Medical Association: 107-134

Nilsson, G.E. (1996) Brain and body oxygen requirements of gnathonemus petersii, a fish with an exceptionally large brain. The Journal of Experimental Biology 199: 603–607

Sullivan, J.P.; Lavoué, S.; Hopkins, C.D. (2000) Molecular systematics of the African electric fishes (mormyroidea: teleostei) and a model for the evolution of their electric organs. The Journal of Experimental Biology 203: 665–683

Terleph, T.A. and Moller, P. (2003) Effects of social interaction on the electric organ discharge in a mormyrid fish, Gnathonemus petersii (Mormyridae, Teleostei). The Journal of Experimental Biology 206: 2355–2362

Turner, R.W.; Maler, L.; Burrows, M. (1999). Electroreception and electrocommunication. The Journal of Experimental Biology 202: 1167–1458.

von der Emde, G. (1999) active electrolocation of objects in weakly electric fish. The Journal of Experimental Biology 202: 1205–1215

Contribution by Emmanuel Gilissen  - August 2007



 

 

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