To evaluate the safety factor for flight feather shafts, in vivo strains were recorded during free flight from the dorsal surface of a variety of flight feathers of captive pigeons (Columba livia) using metal foil strain gauges. Strains recorded while the birds flew at a slow speed (approximately 5-6 m s-1) were used to calculate functional stresses on the basis of published values for the elastic modulus of feather keratin. These stresses were then compared with measurements of the failure stress obtained from four-point bending tests of whole sections of the rachis at a similar location. Recorded strains followed an oscillatory pattern, changing from tensile strain during the upstroke to compressive strain during the downstroke. Peak compressive strains were 2.2+/-0. 9 times (mean +/- s.d.) greater than peak tensile strains. Tensile strain peaks were generally not as large in more proximal flight feathers. Maximal compressive strains averaged -0.0033+/-0.0012 and occurred late in the downstroke. Bending tests demonstrated that feather shafts are most likely to fail through local buckling of their compact keratin cortex. A comparison of the mean (8.3 MPa) and maximum (15.7 MPa) peak stresses calculated from the in vivo strain recordings with the mean failure stress measured in four-point bending (137 MPa) yields a safety factor of between 9 and 17. Under more strenuous flight conditions, feather stresses are estimated to be 1.4-fold higher, reducing their safety factor to the range 6-12. These values seem high, considering that the safety factor of the humerus of pigeons has been estimated to be between 1.9 and 3.5. Several hypotheses explaining this difference in safety factor are considered, but the most reasonable explanation appears to be that flexural stiffness is more critical than strength to feather shaft performance.