Why some bird brains are larger than others

Copyright © 2005 Elsevier Ltd All rights reserved.

Correspondence

Why some bird brains are larger than others

Fahad Sultan

Department of Cognitive Neurology, Hertie-Institute for Clinical Brain Research, University of Tuebingen, Otfried-Mueller-Strasse 27, 72076 Tuebingen,Germany.

Available online 6 September 2005.

Article Outline

Supplemental data

References

How does brain size and design influence the survival chances of a species? A large brain may contribute to an individual’s success irrespective of its detailed composition. I have studied the size and shape of cerebella in birds and looked for links between the bird’s cerebellar design, brain size and behavior. My results indicate that the cerebellum in large-brained birds does not scale uniformly, but occurs in two designs. Crows, parrots and woodpeckers show an enlargement of the cerebellar trigeminal and visual parts, while owls show an enlargement of vestibular and tail somatosensory cerebellar regions, likely related to their specialization as nocturnal raptors. The enlargement of specific cerebellar regions in crows, parrots and woodpeckers may be related to their repertoire of visually guided goal-directed beak behavior. This specialization may lead to an increased active exploration and perception of the physical world, much as primates use of their hands to explore their environment. The parallel specialization seen in some birds and primates may point to the influence of a similar neuronal machine in shaping selection during phylogeny.

The cerebellum is a highly conserved part of the brain present in most vertebrates [1], well suited for a comparative study of size and design. The cerebellum in birds, as in mammals, consists of a strongly folded, thin sheet of gray matter, located dorsally to the brainstem. In birds, it largely consists of a single narrow strip that varies in different species in the antero-posterior extension, which corresponds to the cerebellar length. The cerebellum of birds is commonly subdivided into ten groups of folds termed lobuli [2]. Both variability and regularity are evident in the lobular pattern of the bird cerebella. To quantify these structural varieties and relate them to functional or phylogenetic differences, a principal component analysis was performed on the residuals of the lobuli length, obtained from a double-logarithmic regression of lobuli length against body size (see Supplemental Data on-line for further details).

figure1
Figure 1. Multivariate analysis of cerebellar lobuli lengths in birds obtained from line drawings in [2,10] (see
Supplemental Data for further details).

The graph plots scores of the individual birds on the first two PCs. The two PCs explain 66% of the variance (PC1, 44%; PC2, 22%). The largest variation along the first PC is between the woodpeckers, crows and parrots on the one hand, and the pheasants (Partridge and Wild turkey) on the other. Owls loaded high on the second PC, while swifts and hummingbirds loaded low. Generally, birds were clustered according to their family grouping as seen in the owls (#51), ducks (#14), pigeons (#60), woodpeckers (#17), crows (#123), parrots (#45), and gulls (#82). A one-way factorial ANOVA showed a statistically significant effect of family grouping as a factor on the overall variance (Fratio 4.59, p < 0.001). Two species, the barn owl and mallard, were present in both sources [2 and 10] and are plotted with interconnected dashed lines. Two individuals of the rock dove were present in [10] and are also plotted separately and interconnected by a dashed line. (Numbering of bird families taken from [11] and listed in Table S1 in Supplemental Data.)



Generally, birds within a family (Figure 1) tended to score similarly on the two principal components (PCs). The variability in the principal plane is dominated by variability between bird families (one-way ANOVA with bird family as factor: F(23, 24)= 4.59, p<0.001). The group of birds that scored highly on the first PC consisted of crows, parrots and woodpeckers. In contrast, the nocturnal owls had a different growth pattern and scored highly on the second PC. Both PCs together explained 66% of the total variance (first PC, 44%; second PC, 22%). The cerebellar growth of the first group is based on the enlargement of Larsell’s lobuli IV and VI–IX, while in the owl group lobuli I–II and X increase in size (Figure 2A,B). The difference in enlargement of these two groups of lobuli in the two groups of birds, i.e., crows, parrots and woodpeckers versus owls was statistically significant (Figure 2C).


figure2
Figure 2. Two groups of lobuli contributing to different growth patterns in birds.

(A) Loadings of the individual lobuli on the first two PCs. Evident are two groups: lobuli IV, VI–IX load strongly on the first PC, while lobuli I, II and X load on the second PC. (B) Two birds with roughly equal body size that correlate with the two groups of lobuli are shown (longeared owl, 276 g; green woodpecker, 195 g). In (A,B) contributions of the lobuli to the two first PCs are color coded: red codes first PC, blue second PC. (C) Comparison of the residuals of the two lobuli groups in the owl and in the crow, parrot and woodpecker group. The summed length of the lobuli that loaded highest on either the first or second PC were taken (PC1, IV, VI–IX; PC2, I, II and X) and the residuals to body weight were calculated. Residuals from birds (n = 12) from families that loaded strongly on either the first (crows, parrots and woodpeckers) or second PC (owls) were taken. The difference between these bird groups were statistically significant (t test for lobuli IV and VI–IX: p < 0.001, df = 10; lobuli I, II and X: p < 0.01, df = 10). Error bars: ±SD. Bird drawings taken from [12].


The following groups of cerebellar lobuli can be related to functional subdivisions through their afferents: somatosensory (tail, III–IV; leg, IV–V; wing, IV–VIa; head, V–VII and VIIIb–IXa) [3 and 4], visual (VIc–IXc) [5 and 6], auditory (VII–VIII) and vestibular (IXd–X) [7]. My analysis indicates that, in the diurnal bird group (crows, parrots and woodpeckers), the cerebellar regions that receive visual and trigeminal inputs show the greatest growth, while in the nocturnal owl’s group the vestibular and tail somatosensory receiving regions show the greatest enlargement. The lobuli that are enlarged in crows, parrots and woodpeckers (IV and VI–IX) contribute to about 73% of the overall cerebellar length in birds. Not surprisingly, the birds that have enlarged this part of the cerebellum also have the longest cerebella — normalized for their body weight. The residuals of total cerebellar length in the crow, parrot and woodpecker families were significantly larger than those for the owl families (0.15±0.04 compared to 0.04±0.07, t test p<0.01, df=10).

One unexpected observation was that in excellent flyers only the buzzard scores positively, and that several birds with excellent flying capabilities like the swift and falcon score negatively in the principal plane (Figure 1). This implies that well-developed motor skills per se do not require a large cerebellum, contradicting the common idea that cerebellar size increase in birds is mainly linked to their flying capabilities.

What could be the behavioral denominator common to crows, parrots and woodpeckers that is not developed in owls? All of these birds also have large brains; however, their cerebellar designs differ arguing against a simple co-enlargement model [8]. The enlargement of specific visual and beak-related cerebellar parts in crows, parrots and woodpeckers fits well with their marked adeptness in using their beaks and/or tongues to manipulate and explore external objects. Their skills are even comparable to those of primates in using their hands [9]. The tight temporal coupling between motor command, expected sensory consequences and resulting afferents during visually guided hand and beak usage may be the reason why these animals need large cerebella. The comparative analysis of the birds cerebella reveals that some brains may have enlarged to solve similar problems by similar means during phylogeny. Furthermore it shows that large brains have a specific architecture with dedicated building blocks.

References

1 V. Braitenberg, D. Heck and F. Sultan, The detection and generation of sequences as a key to cerebellar function: experiments and theory, Behav. Brain Sci. 20 (1997), pp. 229–245.

2 O. Larsell, The development and subdivisions of the cerebellum of birds, J. Comp. Neurol. 89 (1948), pp. 123–189.

3 D.G. Whitlock, A neurohistological and neurophysiological study of afferent fiber tracts and receptive areas of the avian cerebellum, J. Comp. Neurol. 97 (1952), pp. 567–635.

4 J.J. Arends and H.P. Zeigler, Cerebellar connections of the trigeminal system in the pigeon (Columba livia), Brain Res. 487 (1989), pp. 69–78. Abstract | PDF (971 K)

5 P.G. Clarke, The organization of visual processing in the pigeon cerebellum, J. Physiol. 243 (1974), pp. 267–285.

6 J.M. Wild, Direct and indirect “cortico”-rubral and rubro-cerebellar cortical projections in the pigeon, J. Comp. Neurol. 326 (1992), pp. 623–636.

7 D.R.W. Wylie, K.L. Lau, X.H. Lu, R.G. Glover and M. Valsangkar-Smyth, Projections of Purkinje cells in the translation and rotation zones of the vestibulocerebellum in pigeon (Columba livia), J. Comp. Neurol. 413 (1999), pp. 480–493.

8 B.L. Finlay, R.B. Darlington and N. Nicastro, Developmental structure in brain evolution, Behav. Brain Sci. 24 (2001), pp. 263–278.

9 L. Lefebvre, N. Nicolakakis and D. Boire, Tools and brains in birds, Behaviour 139 (2002), pp. 939–973.

10 K Senglaub, Das Kleinhirn der Vögel in Beziehung zu phylogenetischer Stellung, Lebensweise und Körpergröße, nebst Beiträgen zum Domestikationsproblem, Z f Wiss Zool 169 (1964), pp. 2–63.

11 G.C. Sibley and B.L. Monroe, Distribution and Taxonomy of Birds of the World, Yale University Press, New Haven (1990).

12 J.F. Naumann, Naturgeschichte der Vögel Mitteleuropas, 2nd edn, Fr. Eugen Koehler, Gera-Untermhaus (1905).

Supplemental data

Corvid cognition

Copyright © 2005 Elsevier Ltd All rights reserved.

Nicola Clayton and Nathan Emery

aDepartment of Experimental Psychology and Sub-department of Animal Behaviour, University of Cambridge, Cambridge, UK

Available online 7 February 2005.

Article Outline

What is a corvid? There are just over 120 species of corvids, a family of songbirds that includes the crows, ravens, rooks and jackdaws, as well as the more colourful jays, magpies and nutcrackers. Although belonging to the same order as nightingales and other birds with melodious songs (Oscines), corvids tend to be identified by their raucous calls. Little is known about corvid songs, perhaps because they are surprisingly quiet. Corvids can be found throughout the globe, except for the southern most tip of South America and the polar ice caps. In Britain, many of the common species, such as magpies and crows, steal other birds’ eggs and raid agricultural crops. They are therefore treated with disdain by many birdwatchers and farmers.

Why study intelligence in crows? Corvids have not always had such a bad press. Native Americans believed that a raven had created the earth; the Norse god, Odin, consulted two ravens Hugin (Thought) and Munin (Memory) for their wisdom; and Aesop cast corvids as the smart protagonists in many of his fables. Along with their reputation in folklore as the wisest of animals, corvids have the largest brains for their body size of any bird. Perhaps most surprisingly, the crow brain is the same relative size as the chimpanzee brain. Other aspects of corvid biology also give us clues to their intelligence. In the wild, young corvids have an extensive developmental period before they become independent from their parents. This allows them more opportunities to learn the essential skills for later life. Many corvids also live in complex social groups. For example, in the cooperatively breeding Florida scrub-jay, several closely related family members share the responsibility of raising the young with the parents. Furthermore, rooks congregate in large colonies, where juveniles associate with many non-relatives as well as kin. In both cases, this long developmental period provides increased opportunities for learning from many different group members.

Perhaps it is not surprising then that many corvids are also renowned for their innovative feeding skills. For example, Japanese crows in Sendai City have learned to crack nuts safely by dropping them onto pedestrian crossings and waiting until the traffic lights turn red before retrieving the nut’s contents. Rooks at a motorway service station in England have discovered a novel method for gaining access to food thrown in rubbish bins. Two birds cooperate in pulling up the bin liner and then either feeding from the raised food or tossing the contents onto the ground where the waiting crowd of colony mates reap the rewards.

As the crow flies… Most of the corvids that have been studied in detail hide food for the future in times of food abundance and then rely on memory to recover the food caches at a later date when food is scarce. For example, the Clark’s nutcracker is estimated to hide over 30,000 pinyon seeds in many different places during the autumn in preparation for the harsh months ahead. Laboratory experiments have shown that they have highly accurate spatial memories, which enable them to recover these caches up to 9 months later. This is no mean feat when there are so many caches to keep track of, scattered throughout the territory, and when many aspects of the landscape change so dramatically across seasons. It has been suggested that Clark’s nutcrackers rely on remembering the location of large vertical landmarks such as trees and rocks in the environment, because these landmarks are unlikely to be blown away or buried under the snow.

What do scrub-jays recall about past caching events? Although western scrub-jays do not hide as many seed caches as the nutcrackers, they are known to cache a variety of perishable foods, such as insects and fruit, as well as non-perishable nuts and seeds. In the laboratory, these birds demonstrate remarkable memories for what they have cached on a given day, and how long ago, as well as where they hid the various food items during that particular caching episode. This ability to remember the ‘what, where and when’ of specific past events is thought to be akin to human episodic memory, because it involves recalling a particular episode that has happened in the past. Until recently, this ability was thought to be unique to humans.

Avian espionage… Food-caching is a risky strategy, however, because the caches can be stolen by other birds. In addition to hiding their own food caches, corvids also play the role of thief: they watch and remember where other birds have hidden their caches and use this information to steal those caches when the owner has left the scene. When playing the role of thief, speed is of the essence and may make the difference between a successful raid and vicious attack by the owner of the food-cache. Not surprisingly, corvids also employ a number of counter strategies to reduce the risk that their own caches will be stolen by another bird. For example, they attempt to cache out of sight from potential thieves, or wait until the raider is distracted before hiding their caches, and if that is not possible, they hide caches in places that are difficult for the thief to see. When there is little option but to cache when others are around, then the birds will return to the caches once the others have left, and quickly re-hide any remaining caches in new places unbeknown to the potential raider.

Laboratory experiments have established that western scrub-jays use all these techniques to protect their caches from potential thieves, and only do so if another bird is present at the time of caching. Furthermore, they only move their caches to new hiding places if they have been thieves themselves in the past. Naı̈ve jays, even ones who have watched other birds caching but have never had the opportunity to raid those caches, do not do so. This suggests that experienced birds relate information about their previous experience of being a thief to the possibility of future theft by another bird, and adjust their caching behaviour accordingly. Using your own experience to predict another individual’s future behaviour in relation to your own – ‘putting yourself in someone else’s shoes’ – is thought to be one of the hallmarks of Theory of Mind, another ability that was thought to be uniquely human.

Cultural tool use in crows? New Caledonian crows are extraordinarily skilled at making and using tools. In the wild, they make two types of tool. The hooked tools consist of twigs that are trimmed and sculpted into a functional hook, which the crows use to poke insect larvae out of tree holes. The crows also manufacture stepped-cut Pandanus leaves, which they use in different ways for different jobs: they make rapid back and forth movements for prey under soil, yet slow deliberate movements if the prey is in a hole. These tools are consistently made to a standardized pattern and carried around on foraging expeditions. The only other animals that display this diversity and flexibility in tool use and manufacture are the great apes. Thus, chimpanzees have been observed to manufacture a range of different tools that are used for specific purposes, and different geographical populations of chimpanzees use different tools for different uses, suggesting that there may be cultural variations in tool use. Observations of the crows’ tool use in the wild also suggest similar levels of cultural complexity. For example, there is potential cumulative evolution in the complexity of stepped tools (increasing the number of steps required to make a more complex tool), analogous to minor technological innovations in humans. Crows from different geographical areas have different designs of tool, suggesting that crows may also show cultural variations in tool use.

Laboratory experiments confirm the sophisticated intellectual capabilities of these crows. One tool-using crow, called Betty, can manipulate novel man-made objects to solve a problem, such as reaching food in a bucket only accessible by using a hook to pull the bucket up. When the bent wire was stolen by another bird, Betty found a piece of straight wire that was lying on the floor, bent this wire into a hook and used it to lift up the bucket and reach the food! Betty proceeded to do this consistently. Furthermore, when given a tool box containing a variety of different tools to reach normally inaccessible food, she was able to select one of the correct length and width. So evidence of tool use and manufacture suggests that these crows can sometimes combine past experiences to produce novel solutions to problems.Feathered apes? Corvids are large-brained, social birds. They have an extensive developmental period in which they are dependent on their parents, and so have a long time-window in which to learn many different things from their parents and peers. They show a great propensity to find innovative solutions to novel problems, from the manufacture of tools to the protection of food from competitors. Furthermore, they appear to be particularly adept at predicting the future behaviour of conspecifics. These features are things they share in common with the apes. The common ancestor of mammals and birds lived over 280 million years ago, so it is hardly surprising that they have very different brains. It follows that intelligence in corvids and apes must have arisen independently in two groups with very different brains. Interestingly, the thinking part of the brain is correlated with propensity to innovate in both birds and primates, with the corvids and apes as the ‘star inventors’. So when it comes to intelligence, corvids are feathered apes.

Further reading

Where can I find out more?

R.P. Balda, A.C. Kamil and P.A. Bednekoff, Predicting cognitive capacities from natural histories: examples from four corvid species, Curr. Ornithol. 13 (1996), pp. 33–66.

N.S. Clayton, T.J. Bussey and A. Dickinson, Can animals recall the past and plan for the future?, Nat. Rev. Neurosci. 4 (2003), pp. 685–691.

N.J. Emery and N.S. Clayton, The mentality of crows: Convergent evolution of intelligence in corvids and apes, Science 306 (2004), pp. 1903–1907.

Heinrich, B. (1999). The Mind of the Raven (Harper Collins).

G.R. Hunt and R.D. Gray, Diversification and cumulative evolution in New Caledonian crow tool manufacture, Proc. Roy. Soc. Lond. B. 270 (2003), pp. 867–874.

L. Lefebvre, S.M. Reader and D. Sol, Brains, innovations and evolution in birds and primates, Brain Behav. Evol. 63 (2004), pp. 233–246.

A.A.S. Weir, J. Chappell and A. Kacelnik, Shaping of hooks in New Caledonian crows, Science 297 (2002), p. 981

“Reprinted from Current Biology, Vol 15 / Issue No 3, Author(s) Nicola Clayton and Nathan Emery, Corvid cognition, Page No. 1, Copyright 8 February 2005, with permission from Elsevier.”
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