For half a century, variation in genome size (C-value) has been an unresolved puzzle in evolutionary biology. While the initial "C-value paradox" was solved with the discovery of noncoding DNA, a much more complex "C-value enigma" remains. The present study focuses on one aspect of this puzzle, namely the small genome sizes of birds. Significant negative correlations are reported between resting metabolic rate and both C-value and erythrocyte size. Cell size is positively correlated with both nucleus size and C-value in birds, as in other vertebrates. These findings shed light on the constraints acting on genome size in birds and illustrate the importance of interactions among various levels of the biological hierarchy, ranging from the subchromosomal to the ecological. Following from a discussion of the mechanistic bases of the correlations reported and the processes by which birds achieved and/or maintain small genomes, a pluralistic approach to the C-value enigma is recommended.