Functional morphology and integration of corvid skulls - a 3D geometric morphometric approach

Background: Sympatric corvid species have evolved differences in nesting, habitat choice, diet and foraging. Differences in the frequency with which corvid species use their repertoire of feeding techniques is expected to covary with bill-shape and with the frontal binocular field. Species that frequently probe are expected to have a relatively longer bill and more sidewise oriented orbits in contrast to species that frequently peck. We tested this prediction by analyzing computed tomography scans of skulls of six corvid species by means of three-dimensional geometric morphometrics. We (1) explored patterns of major variation using principal component analysis, (2) compared within and between species relationships of size and shape and (3) quantitatively compared patterns of morphological integration between bill and cranium by means of partial least squares (singular warp) analysis. Results: Major shape variation occurs at the bill, in the orientation of orbits, in the position of the foramen magnum and in the angle between bill and cranium. The first principal component correlated positively with centroid-size, but within-species allometric relationships differed markedly. Major covariation between the bill and cranium lies in the difference in orbit orientation relative to bill-length and in the angle between bill and cranium. Conclusion: Corvid species show pronounced differences in skull shape, which covary with foraging mode. Increasing bill-length, bill-curvature and sidewise orientation of the eyes is associated with an increase in the observed frequency in probing (vice versa in pecking). Hence, the frequency of probing, bill-length, bill-curvature and sidewise orientation of the eyes is progressively increased from jackdaw, to Eurasian jay, to black-billed magpie, to hooded crow, to rook and to common raven (when feeding on carcasses is considered as probing). Our results on the morphological integration suggest that most of the covariation between bill and cranium is due to differences in the topography of the binocular fields and the projection of the bill-tip therein, indicating the importance of visual fields to the foraging ecology of corvids.