1Department of Experimental Psychology, University of Cambridge, Cambridge CB2 3EB, UK
2Sub-department of Animal Behaviour, University of Cambridge, Cambridge CB3 8AA, UK
Available online 20 August 2007.
Of the 120 species of birds in the corvid family, which includes the crows, ravens, magpies and jays, the bare-faced rook is perhaps the most social of them all. At a rookery in Norfolk, for example, winter roosts can number up to 60,000 individuals. The name for a congregation of rooks is a ‘parliament’. In English folklore, parliament is an apt name for rook justice, as it is said that rooks form a circle around a wrongdoer producing a cacophony of calls and caws which can go on for hours until the offender is either attacked and killed or released to live another day. Although only fiction, such tales reflect their canny reputation as thieves and tricksters, as well as possessors of great wisdom.
Like most birds, corvids are monogamous, and the core unit is therefore the mated pair. This pair bond is typically for life, and the pair remains together throughout the year. For example, rooks and ravens find a partner during the autumn months, taking part in impressive aerobatic displays and food sharing which may be to assess the quality of a potential mate. Once juvenile rooks and ravens pair, they engage in extensive mutual preening and bill twining (bill holding) and support one another in fights.
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 , 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 . 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).
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  and are also plotted separately and interconnected by a dashed line. (Numbering of bird families taken from  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).
(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 .
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) . 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 . 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 . 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.
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