Conventional wisdom holds that depletion of finite oocyte stores is the prime mover in reproductive aging in female birds and mammals. This idea remains pervasive, despite 1. published evidence that some laboratory rat strains reach infertility with a considerable pool of eggs still in reserve; and 2. little rigorous comparative testing. Ovarian declines may be secondary in some species to decaying function of the hypothalamic-pituitary-ovarian (HPO) axis or other factors. We are comparing key aspects of female reproductive aging in distantly-related, similar-sized laboratory birds: the short-lived (6 yrs maximum) Japanese quail, which becomes infertile in its second year of life, and the long-lived (20 yrs maximum) budgerigar parakeet, in which breeding declines after several years. Aged quail hens, like domestic chickens, indeed appear to have depleted numbers of primary ovarian follicles, as predicted by the oocyte depletion model. However, non-laying, aged female budgies retain apparently ample stores of eggs. Our data suggest that absolute oocyte numbers are not a reliable indicator of the ability of to mount a viable hierarchy of ovarian follicles and ovulate successfully. We suggest a modified paradigm for reproductive aging in female homeotherms, both birds and mammals, incorporating a stronger emphasis on early aging cues apart from oocyte stores.