Aortic smooth muscle cells from atherosclerosis-susceptible White Carneau (WC) pigeons lack a functional low density lipoprotein (LDL) receptor pathway. The purpose of the present study was to determine if atherosclerosis-resistant Show Racer pigeons (SR) shared this lack of an LDL receptor pathway and if LDL from normal and hypercholesterolemic pigeons were metabolized similarly. The amount of LDL bound, internalized, and degraded by skin fibroblasts, embryo fibroblasts, and aortic smooth muscle cells from WC and SR pigeons were similar and averaged from 2% to 25% of that seen with monkey smooth muscle cells incubated with the same LDL. LDL uptake by pigeon cells was due largely to nonspecific processes, while specific uptake predominated in monkey cells. A similar lack of specific uptake was obtained with LDL from normal and hypercholesterolemic pigeons. Sterol synthesis and HMG-CoA reductase activity were 10- to 35-fold higher in pigeon cells than in monkey cells incubated in serum-containing medium. LDL had little effect on cholesterol esterification and cholesteryl ester accumulation in pigeon cells. These results indicate that despite major changes in the size and composition of LDL from hypercholesterolemic pigeons, this LDL, like normal pigeon and monkey LDL, was not metabolized by specific uptake processes by pigeon cells. Cells from both WC and SR pigeons lack a functional LDL receptor pathway.